Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum (=Ustilago violacea)

Abstract

The mating system of Microbotryum violaceum was investigated in populations that are polymorphic for mating-type bias, where individuals produce viable haploids of only one of the two required mating types. The cause of mating-type bias was identi®ed as deleterious recessive alleles linked to mating type. Maintenance of the deleterious alleles was promoted by early conjugation among products of single meioses, such that the duration of the free-living haploid stage is minimized. This development was also observed in nonbiased isolates. As a consequence, the mating system tends toward mating within the tetrad, which might be expected to reduce heterozygosity. However, complete centromere linkage of mating type ensures conjugation between ®rst division meiotic products, such that mating in M. violaceum is analogous to forms of meiotic parthenogenesis with ®rst division restitution (i.e. automixis with central fusion). This fungus was used to test the prediction that this mating system would maintain heterozygosity in regions of the genome linked to centromeres. Therefore, populations were screened for additional heterozygous lethal recessive alleles linked to centromeres, and several examples were found. Furthermore, the occurrence of intratetrad mating in M. violaceum provides an explanation for low variation among individuals within populations, inconsistent estimates of outcrossing rates, low levels of mating between tetrads of one diploid individual, and high frequencies of haplo-lethal alleles in natural populations.

Population genetics of fungal diseases of plants

“…In M. violaceum, diploid spores are dispersed and only one may arrive at a time on a given flower, and because further dispersal of the haploid products of spore germination and meiosis is limited, selfing may often be the only option available. Some data however also indicate that a preference for selfing versus outcrossing exists Hood & Antonovics, 2000), that is mediated through developmental patterns that favour intra-tetrad mating (Hood & Antonovics, 2000). At the opposite extreme, the ascomycete pathogen Cryphonectria parasitica, responsible for the chestnut blight, provides an example of a predominantly outcrossing mating system (Marra et al, 2004).…”

Patterns of within population dispersal and mating of the fungus Microbotryum violaceum parasitising the plant Silene latifolia

“…Each of these cells buds off yeast-like sporidia and new infectious dikaryons are produced by conjugation of two cells of opposite mating types. M. violaceum has been studied as an experimental model species in genetics (reviewed in Garber and Ruddat, 2002), host-race differentiation (eg Biere and Honders, 1996;Shykoff et al, 1999;Bucheli et al, 2000), and sex-ratio distortion (Kaltz and Shykoff, 1997;Oudemans et al, 1998;Hood and Antonovics, 2000;Thomas et al, 2003). M. violaceum has also been the basis for theoretical models on transmission dynamics (eg Thrall et al, 1993;Antonovics et al, 1994Antonovics et al, , 1995Thrall and Antonovics, 1995).…”

“…Further, the mating system of M. violaceum exhibits several intriguing peculiarities, with important evolutionary consequences. M. violaceum dikaryons can be produced by selfing in two distinct ways: through intratetrad ( ¼ intrameiotic) or through intertetrad matings (Hood and Antonovics, 2000), and the relative importance of outcrossing, intertetrad selfing and intratetrad selfing in natural populations is not fully known. As intratetrad matings maintain more heterozygosity than intertetrad matings (Kaltz and Shykoff, 1997;Hood and Antonovics, 2000), the occurrence of intratetrad selfing can reduce the deleterious effect of inbreeding.…”

“…M. violaceum dikaryons can be produced by selfing in two distinct ways: through intratetrad ( ¼ intrameiotic) or through intertetrad matings (Hood and Antonovics, 2000), and the relative importance of outcrossing, intertetrad selfing and intratetrad selfing in natural populations is not fully known. As intratetrad matings maintain more heterozygosity than intertetrad matings (Kaltz and Shykoff, 1997;Hood and Antonovics, 2000), the occurrence of intratetrad selfing can reduce the deleterious effect of inbreeding. From an experimental point of view, this also renders difficult the inference of outcrossing rate from the knowledge of heterozygosity, as can typically be done in population genetics studies of other species.…”

Heterozygozity maintenance for the lethals in populations reproducing by intratetrad mating

“…Изучение природных популяций этого гриба показало, что в них с вы-сокой частотой присутствуют летали, сцепленные с локусом типа спа-ривания или с центромерами других хромосом (Hood, Antonovics, 2000). Летали были найдены и в популяциях других грибов со сходным типом размножения.…”